Time-resolved transcriptomics reveals sex-specific programs of gametogenesis and post-spawning gonadal remodeling in the sea cucumber Apostichopus japonicus.

Abstract

The sea cucumber Apostichopus japonicus is an important mariculture species in East Asia, yet the temporal programs that distinguish female and male gonadal development remain incompletely resolved. Histological staging and RNA sequencing were combined to profile female and male gonads across five histologically defined gonadal developmental stages (stages a-e), spanning recovery/resting, proliferation/early differentiation, growth/vitellogenesis, maturation, and post-spawning degeneration/remodeling. Thirty libraries were generated from ten sex-by-stage groups, with three pooled biological replicates per group. Male gonads underwent extensive transcriptional remodeling after stage a, whereas the largest female shift occurred between the recovery and post-spawning stages. Stage-matched comparisons identified 1310, 609, 1436, 4733, and 7578 differentially expressed genes at stages a, b, c, d, and e, respectively, showing that sex-biased expression expanded sharply during maturation and after spawning. Gene Ontology (GO) and Kyoto Encyclopedia of Genes and Genomes (KEGG) enrichment, together with gene set enrichment analysis (GSEA), associated female development with DNA replication, cell-cycle progression, oocyte maturation, lysosomal degradation, glycosaminoglycan turnover, and extracellular-matrix remodeling. Male development was characterized by cytoskeletal reorganization, microtubule and axoneme assembly, ciliary/flagellar movement, motor proteins, lipid metabolism, and energy metabolism. Short Time-series Expression Miner (STEM) and weighted gene co-expression network analysis (WGCNA) resolved distinct temporal profiles and complementary co-expression modules associated with early/recovery, female stage-e remodeling, and male stage-e axoneme/motility patterns. Representative genes associated with these patterns included vasa/DDX4, PIWIL1, nanos1, CDK1, CCNB2, CCNB3, PLK1, TEKT3, CFAP61, DNAH5, CTSF, and ITGB1. These data provide a stage-resolved transcriptomic framework for gametogenesis and post-spawning gonadal remodeling in A. japonicus.